Oral Health conditions in hemodialysis Patients

— Objectives: This study aimed to assess oral health status and self-perceived oral health in hemodialysis (HD) patients. Materials and Methods: Thedecayed, missing and filled teeth (DMFT) index and the community periodontal (CPI) index were used to assess oral health status and self-perceived oral health in 128 HD patients.Salivary flow (SF) and pH were also measured. Results: Mean age was 56.2±17.1 years and mean DMFT was 23±9.14. There were 41 (32%) edentulous participants and 81 (94.3%) non-edentulous participants presented periodontal alterations. SF was normal (≥1.0ml/min) in five (3.9%) participants before HD and in 17 (13.3%) participants after HD. SF was very low (≤ 0.3ml/min) in 6 0 (46.9%) participants before HD and in 26 (20.3%) participants after HD. The difference in SF before (0.39±0.28ml/min) and after (0.60±0.34ml/min) HD was significant (p<0.001). There was a negative correlation between salivary flow and age before (r=-0.188, p=0.033) and after (r=-0.261, p=0.003) HD. Conclusions: Despite the increase in salivary flow after HD sessions, the rates were still below the normal levels, thus indicating the need for special care. Clinical Relevance: Our findings show that the oral health care professional should provide preventive and restorative treatment to HD patients and should be included in themultiprofessionalhealth team managing the care of HD patients.


INTRODUCTION
Chronic kidney disease (CKD) is a progressive condition characterized by a gradual loss of kidney function over time. Its diagnosis is made on the basis of decreased glomerular filtration rate or markers of kidney damage, or both, of at least 3 months duration [1]. Early recognition and intervention are essential to slowing disease progression, maintaining quality of life, and improving outcomes [2]. are very susceptible should be part of their treatment. Failure to do so can lead to the onset of infectious diseases thatinterfere with the treatment and/or even delaykidneytransplant [9].
The saliva, which plays a major role in digesting food and in preserving the integrity oforal tissues, can be negatively affected inpatients with kidney failure.However, few studies have evaluated salivarychanges and composition in patients undergoing HD [10,11].Research has shown that fluid intake restriction, use of different types of drugs, systemic disorders and radiation therapy are specific risk factors for changes insalivary pH and flow [12].
Although HD therapy prevents patients from visiting the dentist,it is estimated that 90% of patients with CKDundergoing HD have some oral health problem [13,14]. The most common oral health problems in this population are gingival inflammation, increasedperiodontal probing depth, xerostomia, halitosis anddental caries [5,15,16].Moreover, many patients do not perceive the need for preventive dental care,andsystematic oral health education programs targeted at HD patients have not been described in the literature [17,18].
Thus, considering the hypothesis that HD can modify the oral environmentin the long term andimmediately after the treatment session, understanding the changes in the salivary flow andthe oral health conditions related to HD may improvehealthcare professionals'decisionmakingregarding treatment protocols for these patients. Given that, the present study aimed to assess the oral health status, including dental problems, soft tissue and salivary (flow and pH) changes, and the self-perceived oral healthof patients undergoing hemodialysis.

II. MATERIALS AND METHODS
A cross-sectional study was conductedin two hemodialysis clinicslocated ina capital city in Northeastern Brazil. Data were collected in 2013 and these clinics were selected for being reference hemodialysis treatment centers. Data were collected in three phases by a single researcher (PLPM) who was trained by a co-author (ABL) for phase twoand calibrated against a gold standard examiner (MVLS) for phase three (intra and inter kappa values were>0.8). In the first phase, an interview was conducted to obtain information on patients'self-perceived oral health status.The questionnaire was adapted from a World Health Organization's Oral Health Survey [19]and included questions regarding oral pain, dry mouth, difficulty swallowing, problems with the taste of food, and burning mouth sensation.Additionally, data onparticipants'general health and socioeconomic status were collected from medical records.
The second phasewas designed to assess salivary flow and pH.The participants were aware of the required abstinence from smoking, drinking, eating and tooth brushing at least one hour prior to saliva collection. This phasetook place at two moments: immediately before and immediately after the hemodialysis session.Salivary pH was measured using pH indicator strips (pH 0-14; Merck®, Darmstadt, Germany). The patient was asked to remain with the mouth open and a strip was placed on the tongue for one minute. After removing the strip, the color change was compared with the color chart and recorded in the patient's file [20].
The analysis of salivary flow was performed with saliva collected after stimulation. This procedure is useful forallowingsaliva collection from major and minor salivary glands [21]. Patients were asked to chew a piece of sterile rubber sheet (3 cm x 2 cm),which is used in dental procedures, for one minute.The rubber sheet was tied to dental floss to prevent swallowing. The first sample of saliva collected immediately after stimulation was discarded. After that, the patient was asked to spit into a glass container graduated in milliliters for five minutes and the amount of saliva collected was divided by the time the collection process lasted, thus providing the salivary flow rate in mL/min [22].Stimulated salivary flow rates that ranged 1-3 mL/minute were considered normal for adults. Hyposalivation occurred whenthe rate was below 1mL/minute [23,24].Stimulated whole saliva flow rates below 0.7 mL/minute are within the lower range of output and suggest salivary hypofunction [25]. Therefore, the percentage of patients with salivary flow rates below 0.7mL/min was also calculated and studied.
The last phase of data collection consisted ofan oral examinationbefore the hemodialysis session using the following sterilized instruments: flat mouth mirror (size No.5) and the WHO-621 periodontal probe,which has a ball end of 0.5mm diameter and a first colored band at 3.5-5.5mm.Assessment of oral health and oral mucosal status was carried out with the patient sitting on a chair under  [19]. Oral examination was performed, and the data were recorded in about 15-20 minutes.
The data were analyzed using SPSS for Windows (version 19.0,SPSS Inc., Chicago, IL, USA) with a significance level set at 5% (p<0.05). Pearson's correlation test,Fisher's exacttest and one-way ANOVA wereused to analyze the data and checkfor correlations between the variables. Continuous variables were described as median and mean ± standard deviation (SD) and categorical variables were described asfrequencies and percentages.

III. RESULTS
There were155 eligible patients in the HD clinics, but16 were excluded after application of the exclusion criteria and 11refused to participate in the research. Thus, the final sample consisted of 128 patients. Of these, 92 (72.7%) were originally from the state's capital and 36 (27.3%) were from smaller cities.
The age of the participants ranged 20 to 91 years,with a mean age of 56.2±17.1 years and a median age of 59 years. Table 1 shows the socioeconomic status of the participants in the two centers. The patients were predominantly men (n=66; 51.6%), married (n=79; 61.7%), retired(n=64; 50%), had primary education(n=51; 39.8%) and received up to one minimum wage(n=88; 68.8%).
The information collected from the patients' medical records revealed that the disease that more often causedCKDwas hypertension (n=96;75.1%), followed by diabetes (n=47; 36.8%). Other diseases directly related to kidney disorders, such as glomerulonephritis and kidney stone,accounted for26 cases (20.3%). Table 2 shows patient's self-reported oral discomfort, with dry mouth being the patient's major complaint, although it did not significantly correlate with salivary flow before or after hemodialysis (p=0.342 and p=0.404, respectively).  Table 4 shows thatsalivary flow rate before the hemodialysis session ranged 0.10 mL/min to 1.80 mL/min and some patients exhibited a salivary flow rate below 0.7 mL/min. After the session, salivary flow rate ranged 0.10 to 2.0 mL/min, with some patients exhibiting a salivary flow rate below 0.7 mL/min. Salivary flow was normal (≥1.0ml/min) in five (3.9%) patients before the hemodialysis session and in 17 (13.3%) patietnsafter the hemodialysis session.Extremely low salivary flow rates (≤ 0.3ml/min) were found in 60 (46.9%) patients before the HD session and in 26 (20.3%) after theHD session.
Salivary flow differed significantly before and after the hemodialysis session and it was measured using continuous and categorical scales. Increased salivary flow was observed in 106 participants (82.8%) and salivary pH was higher before the HD session(pH 7.18±0.87)compared with the pH after the HD session (pH 6.82±0.78), as shown in Table 4. Table 5presents the significant correlations of changes in salivary flow before and after hemodialysis with age, DMFT and pH. No correlation was observed between duration of hemodialysis treatment and periodontal problems measured by the CPI (rs=0.039. p=0.720) even when comparing the duration of hemodialysis treatment between different periodontal problems groups (one-way ANOVA, p=0.537).
When the correlation between salivary flow and age was analyzed, a negative relationship was found (age and salivary flow before hemodialysis: r=-0.188, p=0.033; age and salivary flow afterhemodialysis: r=-0.261, p=0.003; age and salivary flow difference: r=-0.208, r=0.019), showing that not only salivary flow is decreased with age, but also that the increase of salivary flow after hemodialysis is decreased with age.

IV. DISCUSSION
Patients undergoing hemodialysis (HD) are vulnerable to infection and the oral cavity is a potential source of infection. Therefore, it is important to monitor HD patients' oral health (including salivary flow and sources of infection, such as dental cavities and periodontal problems) and implement oral health preventive measures.
In the general population, the association between salivary flow and age is unclear. While some clinical studieshave shown a reduction in salivary flow with age [26,27], other studies have not reportedsuch association [28,29].However, saliva is a robust indicator for monitoring health status and for disease surveillance as it is a noninvasive, cost-effective andhighly sensitive diagnostic approachthat correlates with blood samples [11].In our study, the association between salivary flow and age revealed that not only salivary flow is decreased with age, but also the improvement of salivary flow after HDproportionally decreased with age. The saliva plays a major role in oral healthand older adults undergoing HDare at increased risk for oral diseases [22].Therefore, this population group needs a higher standard of care to prevent systemic complications caused by oral health problems.
It should be noted that HD patients also present with general and oral health problems (e.g., xerostomia, drug idiosyncrasy, drug side effect) that affect their oral health and quality of life [6,30]. A decrease in salivary flow may result in a significant decline in oral health defense and thus lead to discomfort and clinical problems, such as caries, altered taste, halitosis, and increased susceptibility to infections [22]. Therefore, the dentist should be part ofthe HD care team so that patients arecarefully managed.However, the dentist musthave awide knowledge of HD treatment to better understand how HD can modify oral health status. Some factors are essential for the dental treatment of hemodialysis patients, particularly the evaluation of medical history, medication profile and radiographic and laboratory data [31]. The restorative dentistry treatment should preferably be performed prior to the first HD session [32].However, if this is not possible, dental treatment should be avoided on dialysis daysin order to avoid the interference of the use of local anesthesia with adrenaline, which will demand special care from the health care provider [33].
Patients' low socioeconomic status, as observed in the present study, can increase their vulnerability to health complications.Researchersemphasize that oral diseases are still a major public health problem in high-income countries and a growing problemin many low-and middleincome countries.Socioeconomically disadvantaged groups are atincreased risk for these problems and often do notreceive adequate oral health care. In addition, oral disease prevention is usually neglected in public health services, which, once again, puts patients undergoing HD in public servicesat greater risk for oral health problems [34].
Thesialometry showed a significant increase in salivary flow after the HD session (p<0.001).However, such increase was not enough to place the majority of patients undergoing HD in the normal range of salivary flow seen in healthy patients (0.7 to 1.0 mL/min) [35,36].
Thesefindings are corroborated by studies performed in India and Brazil [10,37]. Salivary flowcorrelated with the DMFT index, thus indicating thatpatients'reduced salivary flow leads to a greater prevalence of dental caries. Reduced salivary flowcompromises taste and swallowingand increases the risk of fungal and bacterial infections [38].It is important to understand that saliva is a fluid with many functions, such as oral digestion, oral mucosa lubrication, maintenance of the ecological balance in the oral cavity, antimicrobial activity and effective protection of teeth integrity by maintaining pH in the oral cavity [39]. Control of oral infections may be hampered if salivary flow and or its function is altered or reduced, which will decrease its lubricating effect and therefore its capacity to maintain the integrity of oral structures [40].
The association between risk factors shared by various disabling conditions requires interventions by national health programs, which can be effective in improving the oral health status and quality of life of population groups [34]. Oral health issues need to be addressed by the public health system, especially whensocioecnomically disadvantaged population groupsare involved. Given that, it should be noted that the HD patients analyzed in the present study are faced with a double burdenthe disease (and all its related problems) and the difficulty to access oral health treatment,which is commonly observed in population groups of low socioeconomic status. A multinational study conducted inFrance, Hungary, Italy, Poland, Portugal, and Spain suggested that the stress deriving from the treatment itself reduces the quality of life and self-care capacity, resulting in worse oral hygienealthough the multifactorial nature of oral diseases is also acknowledged [41,42].
In our study, dentalcaries was evaluated by the DMTF index. The findings regardingpresent (decayed teeth) and past (filled and missing teeth) experiences suggest a poor dental status in the study population. This situation may beindirectly influenced by the kidney disease and by socioeconomic and cultural factors, especially with regard to missing teeth, for which the mean was 18.9±11.7 teeth.Similar findingsregardingedentulismhave been reported in another study [43], and the last national oral health survey in Brazil showed adults with a mean of 7.4 missing teeth [44].
Our data support other findings that chronic kidney disease (CKD) may have significant effects on periodontal health. Although there was no correlation between PCI and HD treatment duration as reported in the literature, changes such as increased dental calculus, gingival inflammation, probing depth and attachment loss were also detected [45,46].Given that, treatment and control of
Although the need for such care is acknowledged, access to dental care in the past year was reported only by 32% of the patients in our study. A similar study of 147 hemodialysis patients in Canada showed that 41% of the participants had undergone dental treatment in the previous year [33]. These findings reinforce the need for greater provision of primary and preventive care by oral health professionals in order to reduce infection and other complications that contribute to increased morbidity and mortality, such as atherosclerotic complications and future transplant rejection [10,47,49].
The present study showed oral and salivary changes in patients undergoing HD. Despite the absence of correlation between salivary flow and oral discomfort, salivary flow (before and after HD) was negatively correlated with age and DMFT and positively correlated with salivary pH.Nevertheless, a high percentage of participants reported some type of oral discomfort. Awareness of the oral health of HD patients is an important strategy to alert dentists about preventive measures aiming to minimize problems that might impair general health status.Oral and salivary changes in HD patients suggest a need for special attention tooral health treatment [10].
Despite not being the main objective of our study, our findings demonstrated the need to include the dentist in the multidisciplinary team responsible for patients undergoing HD. The inclusion of the dentist in the multidisciplinary team should be discussed in HD centers around the world, particularly in public facilities and infacilities that serve patients of low socioeconomic status.
The present study has some limitations. The study did notinclude a control group and did not consider that other external factors may influence oral health, salivary flow and pH measures.Althoughthe findings cannot be generalized to all the patients, changes in the oral health status were found in patients undergoing HD. Therefore, further studies should be carried out to strengthen research in this field.
Our findings demonstrated thatHD patients present with dental and periodontal problems. There was a high prevalence of moderate and severe periodontal disease and a high DMFT index, with a predominance of missing teeth. An association between salivary flow and age was observed, showing that not only salivary flow is decreased with age, but alsothat the improvement of salivary flow after HD proportionally decreased with age. Despite an increase in salivary flow after the hemodialysis session,itsvalueswere still below the normal levels. The oral health care professional should provide preventive and restorative treatment to HD patients and should be included in themultiprofessionalhealth team managing the care of HD patients.